Identification of photoperception and light signal transduction pathways in citrus

Identification of photoperception and light signal transduction pathways

in citrus

Vera Quecini

Instituto Agronômico de Campinas, Centro de Pesquisa e Desenvolvimento de Recursos Genéticos,

Campinas, SP, Brazil.

Abstract

Studies employing model species have elucidated several aspects of photoperception and light signal transduction that control plant development. However, the information available for economically important crops is scarce. Citrus genome databases of expressed sequence tags (EST) were investigated in order to identify genes coding for func-tionally characterized proteins responsible for light-regulated developmental control in model plants. Approximately 176,200 EST sequences from 53 libraries were queried and allbona fide and putative photoreceptor gene families were found in citrus species. We have identified 53 orthologs for several families of transcriptional regulators and cy-toplasmic proteins mediating photoreceptor-induced responses although some importantArabidopsis phytochrome-and cryptochrome-signaling components are absent from citrus sequence databases. The main gene families re-sponsible for phototropin-mediated signal transduction were present in citrus transcriptome, including general regu-latory factors (14-3-3 proteins), scaffolding elements and auxin-responsive transcription factors and transporters. A working model of light perception, signal transduction and response-eliciting in citrus is proposed based on the iden-tified key components. These results demonstrate the power of comparative genomics between model systems and economically important crop species to elucidate several aspects of plant physiology and metabolism.

Key words:cryptochrome, data mining, light signaling, phototropin, phytochrome.

Received: July 21, 2006; Accepted: February 8, 2007.

Introduction

Plant development is highly plastic, allowing the envi-ronment to exert tight control over the transitions between genetic developmental programs in order to maximize growth and reproduction (Meyerowitz, 2002). Light pro-vides spatial and temporal information to regulate plant de-velopment throughout its life cycle: from germination and seedling establishment to the onset of the reproductive stage (Schäfer and Nagy, 2006). Plants are able to detect environ-mental light direction, duration, fluency and wavelength due to a complex system of photoreceptor molecules: the blue (B) and ultraviolet-A (UV-A) 320-500 nm light-sensing cryptochromes (cry) and phototropins (phot) (Banerjee and Batschauer, 2005) and the red (R)/far red (FR) 600-750 nm phytochrome (phy) receptors (Schepenset al., 2004). Re-cently, a novel family of putative B photoreceptors has been described inArabidopsis thaliana: the ZEITLUPE (ZTL)/ Flavin-binding Kelch repeat F-box protein (FKF1)/LOV Kelch Protein (LKP2) family (Nelsonet al., 2000; Schultzet

al., 2001; Somerset al., 2000). ZTL/ FKF1/LKP2 are in-volved in the circadian clock mechanism and photoperiodic flowering response (Imaizumiet al., 2005).

In higher plants, photoreceptor co-action is a com-mon theme and the pathways may function synergistically, antagonistically and additively to control several develop-mental responses (Schäfer and Nagy, 2006). Moreover, plant photoreceptors operate in concert with numerous other signaling systems; including phytohormones, carbo-hydrate-mediated, temperature, gravity and the endoge-nous clock transduction pathways (Halliday and Fankhauser, 2003; Chenet al., 2004; Heggie and Halliday, 2005). The molecular mechanisms involved in light-induced signal transduction include the following: light-re-gulated sub-cellular localization of the photoreceptors (Guoet al., 1999; Nagy and Schäfer, 2002; Chen et al., 2005; Kong et al., 2006); a large reorganization of the transcriptional program (Casal and Yanovsky, 2005; Fran-klinet al., 2005) and light-regulated proteolytic degrada-tion of several photoreceptors and signaling components (Höcker, 2005; Huq, 2006).

Studies employing model plant species have demon-strated that photoperception, the signal transduction path-www.sbg.org.br

Send correspondence to Vera Quecini. Centro de Pesquisa e Desenvolvimento de Recursos Genéticos, Instituto Agronômico de Campinas, Caixa Postal 28, 13001-970 Campinas, SP, Brazil. E-mail: vquecini@iac.sp.gov.br.

ways and the responses elicited by light form a complex interconnected network rather than a linear pathway (Chen et al., 2004; Quecini and Liscum, 2006). The diversity of light responsiveness observed in plants has arisen from the elaboration, combination and re-arrangement of a basic repertoire of mechanisms responsible for light-mediated developmental regulation, allowing adaptation to a wide range of climatic and latitudinal regions. Comparative genomics has provided tools to access the genetic bases of this diversity in non-model species using bioinformatics, which increases the fundamental knowledge of gene inter-actions and permits analyses of the functional significance of proteinsin silico(e.g.Santelli and Siviero, 2001; Souza et al., 2001; Hechtet al., 2005).

Virtually all information about light-regulated devel-opment in woody plants comes from studies withPopulus, a temperate deciduous perennial (Zhu and Coleman, 2001; Olsen and Juntilla, 2002). Adaptive traits in temperate peren-nial woody plants involve an integrated physiological re-sponse directed at plant survival and nutrient storage over the winter period and are greatly dependent of photoreceptor-mediated perception of seasonal progression (Thomas and Vince-Prue, 1997). Surprisingly, recent evidence has dem-onstrated that light is also the main factor triggering the tran-sition between vegetative to reproductive developmental stages of trees in Equatorial regions (Borchertet al., 2005). The effects of light on developmental processes in citrus and other neotropical tree species have been described in several situations, although without approaching the molecular as-pects of the metabolism (Steppeet al., 2006; Chen L-Set al., 2005; Ravehet al., 2003; Tornéet al., 2001). Mutant studies employing transgenically generated plants have demon-strated variable extents of functional conservation in the genes responsible for developmental control between citrus and model species (Penaet al., 2001; Pillitteriet al., 2004). However, the detailed functional characterization of individ-ual genes is a limiting factor in the study of tree species, and new strategies should be devised for the study of gene func-tion (Groover and Robischon, 2006).

Based on evidence of extensive conservation in photo-perception and light signal transduction in angiosperms, this work aimed to identify the characterized components of these pathways in citrus. Our results have demonstrated that a large portion of the genes involved in light responses from model species are present in citrus and that they share extensive pro-tein sequence conservation in several regions, including func-tionally characterized domains. These results demonstrate the potential use of comparative genomic tools to elucidate physi-ological and metabolic processes in crop species.

Material and Methods

Database searches and alignments

Homologs ofArabidopsis thaliana and other model species photoperception and light signal transduction genes

were identified in BLAST searches (Altschulet al., 1997) against EST sequences from the citrus index databases at CitEST, consisting of approximately 176,200 ESTs ob-tained from the sequencing of 53 libraries. Data validation was performed by tBLASTx and tBLASTn searches using BLOSUM80 scoring matrix of the retrieved hits against the databases at NCBI (National Center for Biotechnology In-formation) built inside the CitEST project. Sequences fail-ing to retrieve the original bait sequence were eliminated from the projects. The resulting alignments were filtered by a threshold e-value of 1e-15 and the validated hits were fur-ther analyzed according to functional domain description. Validated sequences were translated and protein (deduced amino acid) alignments were performed using ClustalX (Thompsonet al., 1997). When necessary, alignments were manually adjusted using Lasergene MegAlign (DNASTAR, Madison, WI, USA).

Motif analysis andin silicocharacterization

The identified homologs were investigated for the presence and sequence conservation of recognizable func-tional domains described in several protein analysis and gene function databases (European Bioinformatics Insti-tute-European Molecular Biology Laboratory - EMBL-EBI; Expert Protein Analysis System - ExPaSy from the Swiss Institute of Bioinformatics - SIB; Protein Families database - Pfam).

Phylogenetic analysis

The functionality of citrus genes in comparison to the characterized homologs was assessed by genetic distance and phylogenetic studies. Phylogenetic analyses were per-formed using distance and parsimony methods in the soft-ware PAUP* 4.0b10, using the softsoft-ware default parame-ters. Re-sampling bootstrap trees containing 1000 random samples were constructed using PSIGNFIT software. Mod-ular functional domains were employed for genetic dis-tance studies for genes previously described as having di-vergent regions and conserved blocks.

Results and Discussion

transduction components and light-regulated transcription factors, whereas the remaining 22 are similar to phot signal-ing partners (Figure 1). Homologs from the transcriptional regulators PAT1 (PHYTOCHROME A SIGNAL TRANS-DUCTION 1, AT5G48150) (Bolle et al., 2000), HRB1

(HYPERSENSITIVE TO RED AND BLUE 1,

AT1G02340) (Kanget al., 2005), OBP3 (OBF4-BINDING PROTEIN 3, AT3G55370) (Wardet al., 2005) and from the novel signaling components FHL (FHY1-LIKE, AT5G02200) (Zhou et al., 2005) and SRR1 (SENSITI-VITY TO RED LIGHT REDUCED 1, AT5G59560) (Staigeret al., 2003) were absent from CitEST databases. However, the existence of citrus orthologs cannot be ruled out at this point due to the restricted coverage of the

trans-criptome analysis, the expression levels and patterns of these genes and the post-translational modifications re-quired to generate functional components. InArabidopsis and rice, several genes involved in light signaling have been identified by biochemical, forward and reverse ge-netic assays (Zhouet al., 2005; Keveiet al., 2006)

Photoreceptor-related genes

Citrus EST database contains homologs of members of all families of plant photoreceptors: namely, the phyto-chrome, cryptochrome and phototropin families (Table S1, Figure 2, Figure 3, Figure 4). In higher plants, phy are re-sponsible for the control of major developmental processes, such as seed, germination, de-etiolation, shade avoidance, Figure 1- Functional classification of citrus transcripts associated to photoperception and light signal transduction based on gene ontology (GO)

Figure 2- Domain structure, phylogenetic analyses and alignment of the predicted amino acid sequence of phytochrome family in citrus.

Neigh-bor-joining trees for citrus and tree species deduced amino acid andArabidopsisfull length sequences aligned with ClustalX are shown. Bootstrap values are indicated above each branch. Dark and light gray shading indicate sequence identity and similarity, respectively. At,Arabidopsis thaliana; C Number, contig number; Cit, citrus; CS, Citrus sinensis; CR, Citrus reticulata; FAD, flavin adenosine diphosphate; FR, far-red light; HKRD, histidine

Figure 3- Domain structure, phylogenetic analyses and alignment of the predicted amino acid sequence of the cryptochrome family in citrus. Neigh-bor-joining trees for citrus deduced amino acid andArabidopsisfull length sequences aligned with ClustalX are shown. Bootstrap values are indicated

floral induction and entrainment of the circadian clock (Chenet al., 2004). Four EST singlets sharing sequence similarities to phy family genes were identified; three inC. sinensisand one inC. reticulatagenome (Table S1). Two ofC. sinensisESTs show higher levels of sequence similar-ity toPHYAgenes, whereas the remaining ones are related to PHYB-type of sequences. Interestingly, the PHYB homologs in citrus appear to be more distantly related from thePopulus PHYB1andPHYB2sequences than from theA. thaliana PHYEgene (Figure 2). The branching in thePHYB

genes is a relatively recent event and is absent from many plant species, includingArabidopsis(Mathews, 2006). The partial nature of the sequences prevent us from speculating whether citrus genome has a singlePHYBgene or two, like the current model woody plantPopulus.

The cryptochrome family is represented in the citrus genome by two ESTs corresponding toArabidopsis CRY1 and five sequences similar to CRY-DASH (Table S1, Fig-ure 3). Although, all the identified sequences share similar-ities to higher plant cry sequences, for the majority of them Figure 4- Domain structure, phylogenetic analyses and alignment of the predicted amino acid sequence of phototropin and zeitlupe in citrus.A.

phototropin family.B.zeitlupe family. Neighbor-joining trees for citrus deduced amino acid andArabidopsisfull length sequences aligned with ClustalX are shown. Bootstrap values are indicated above each branch. Dark and light gray shading indicate sequence identity and similarity, respectively. At,

Arabidopsis thaliana; B, blue light; C Number, contig number; CA,Citrus aurantium;Cit, citrus; CS,Citrus sinensis; CR,Citrus reticulata; FAD, flavin adenosine diphosphate; LOV, light, oxygen, voltage subtype of PAS; PT,Poncirus trifoliata; R, red light; STKD, serine/threonine kinase domain; UV-A,

(five), the deduced amino acid sequence identity is re-stricted to the photolyase-like domain (Figure 3), indicating that these genes may function as photolyases rather than bona fideB photoreceptors. The C-terminal extension, es-sential for cry1 function inArabidopsis, is conserved inC. sinensisEST and in C. reticulataEST contig (Table S1, Figure 3). Cryptochromes are mainly responsible for de-etiolation under blue light inArabidopsis, including control of transcriptional regulation, inhibition of hypocotyls growth, promotion of cotyledons expansion, and synthesis of several non-photoreceptor pigments, such as chlorophyll and anthocyanins (Li and Yang, 2006). In addition, this class of photoreceptor acts in coordination with phy to reset the circadian clock and to control the transition to flowering (Yanovsky and Kay, 2002). At least two of the identified sequences (CS00-C1-100-038-A12.CT and C13-CA) are likely to code for functional cry family members in citrus.

InArabidopsis, the phototropin photoreceptor family consists of two closely related members that share almost 60% protein identity. In the genome of citrus species, an EST contig whose deduced amino acid sequence shows 71% identity to PHOT2 and four cDNAs with sequences approximately 50% identical to PHOT1 and PHOT2, were identified (Figure 4A, Table S1). The overall sequence con-servation between citrus and other species PHOT proteins is high, including at the N-terminal LOV domains, essential for chromofore binding and protein function in Arabidopsis,reviewed in Quecini and Liscum (2006). The remaining identified ESTs and EST contigs present high levels of sequence identity restricted to the C-terminal serine/threonine kinase and thus, may not perform photo-perception-related functions. InArabidopsisand rice, phot family controls a specific sub-set of physiological pro-cesses, including phototropic stem curvature, stomata opening control and chloroplast relocation (Quecini and Liscum, 2006). Only recently, phots have been demon-strated to be involved in B-mediated seedling de-etiolation (Foltaet al., 2003; Takemyiaet al., 2005). InArabidopsis, phot1 and phot2 have specialized and overlapping roles, phot1 being the most important photoreceptor sensing di-rectional B under low fluence rates and phot2 responsible for high light responses (Briggs and Christie, 2002). The presence of multiple PHOT-like sequences in citrus ge-nome suggests that such a fluence rate-specific role might occur.

Recently, a three-member family of putative photo-receptors has been characterized in Arabidopsis; the ZTL/FKF1/LKP2 family (Somers, 2001). It is represented by three distinct sequences in citrus genome databases: one highly similar to FKF1 with lower homology to ZTL and two sharing sequence similarity to FKF1 and LKP2 (Table S1, Figure 4B).ArabidopsisZTL/FKF1/LKP2 proteins are characterized by the presence of a flavin-binding LOV do-main at the protein N-terminal, an F-box dodo-main and a stretch of Kelch repeats, providing a direct link between

light perception and ubiquitin-mediated protein degrada-tion. The family has been functionally associated to the endogenous time-keeping mechanism and the control of photoperiodic flowering time (Imaizumi et al., 2003; Imaizumiet al., 2005). InArabidopsis, ZTL and FKF1 are thought to be components of an Skp1-Cullin-F-box (SCF) E3 ubiquitin ligase complex (Vierstra, 2003). ZTL has been implicated in the ubiquitin-mediated proteolytic degrada-tion of the clock component TOC1 (Máset al., 2003) and in the regulation of developmental responses to R, possibly through its interaction with phyB (Keveiet al., 2006), while FKF1 has been demonstrated to control the levels of the photoperiod-sensingCONSTANS(CO) gene via degrada-tion of its transcripdegrada-tional repressor, a DOF type transcrip-tion factor, CDF1 (Imaizumiet al., 2003; Imaizumiet al., 2005).Thus, ZTL post-translationally regulates TOC1 lev-els and FKF1 controls dailyCOexpression in part by de-grading CDF1. Citrus FKF1/ZTL- and LKP2-like EST contigs are highly conserved at the F-box and Kelch repeats domains (Figure 4B), suggesting a function in the prote-lolytic degradation of circadian-clock associated factors.

Phy and cry signal transduction components

Phytochrome responses are associated with changes in gene expression (Casal and Yanovsky, 2005) and mem-bers of several transcription factor families are required for phy signaling or are early targets of phy-mediated re-sponses. In citrus, 22 EST contigs corresponding to the Arabidopsistranscriptional regulators and nuclear factors involved in phy and cry light signaling were identified, along with 17 transcripts associated to light-mediated pro-teolysis and seven transcripts similar to several signaling events of light signaling, such as Ca2+_{-binding and} post-translational protein modification (Figure 1, Table S2).

In Arabidopsis, the PIF (PHYTOCHROME-INTE-RACTING FACTOR) and PIL (PIF-LIKE) family of bHLH (basic Helix-Loop-Helix) transcriptional regulators, which includes HFR1/REP1/RSF1 (LONG HYPOCOTYL

IN FAR RED 1/REDUCED PHYTOCHROME

un-identified factors to regulate transcription of a master set of regulators, such asCCA1(Wang and Tobin, 1998),LHY1 (Schafferet al., 1998),TOC1andCO(Harmeret al., 2000; Teppermanet al., 2001); and (ii) these regulators then con-trol the transcription of genes encoding functions necessary for the terminal steps of the signaling cascade. Interest-ingly, in citrus genome databases, thePIF/PIL/HFRfamily is represented by a single EST contig fromC. aurantifolia and C. latifolia, displaying higher identity to PIF4 and HFR1 protein (Table S2, Figure 5). Another two highly similar EST contigs (55.5% deduced amino acid sequence identity) showed moderate (15.0 to 17.5%) and low (7.5 to 2.9%) identity to HFR1 and PIF/PIL gene products, respec-tively. The functional significance of these transcripts as PIF/PIL/HFR-like light-induced transcriptional regulators remains unclear. The absence of PIF-like transcripts inC. sinensisandC. reticulata transcriptomes, which together correspond to approximately 72% of CitEST database, is noteworthy given their importance in light-mediated re-sponses inArabidopsis.

Several basic domain/zinc finger (Zn finger) and MYB-type factors function as downstream convergent tar-gets of phy and cry signaling inArabidopsis, independently of G-box photoreceptor binding (Oyama et al., 1997; Chattopadhyayet al., 1998; Ballesteroset al., 2001). In cit-rus species transcriptome, six cDNAs corresponding to this class of transcriptional regulators were present: namely, one HY5 (LONG HYPOCOTYL 5), one HYH (HY5-HOMOLOGOUS) and four LAF1 (LONG AFTER FAR RED 1) homologs (Table S2, Figure 6A). Down-regulation of these signaling pathways occurs when phyA and the transcription factors, HY5 and LAF1, are degraded in a light-dependent fashion by the proteasome in a mecha-nism that involves COP1 (CONSTITUTIVELY PHOTO-MORPHOGENIC 1) (Saijoet al., 2003; Seoet al., 2004; Janget al., 2005). The COP9 signalosome (CSN) is also in-volved in HY5 degradation (Penget al., 2001). Moreover, SPA1 (SUPRESSOR OF PHYA-105 MUTATION) and the other members of the SPA family regulate the ubi-quitin-ligase activity of COP1 (Saijoet al., 2003; Seoet al., 2003). In citrus EST databases, COP1, other components of the CSN and a small group of SPA-like transcripts were identified, suggesting the existence of a similar mechanism of phy-mediated signal desensitization route (Table S2, Figure 6B).

Photoreceptor-initiated signaling pathways also con-sist of cytosolic components in Arabidopsis and other model species. General transduction pathways, such as G-protein, Ca+2_{-calmodulin and protein phosphorylation} cascades have been demonstrated to take part in light-triggered signaling (Bowleret al., 1994). Homologs of sev-eral Ca+2_{-binding and protein phosphorylation factors in} phy- and cry-initiated signal transduction were identified in citrus transcriptome (Table S2). Phosphorylation may be

responsible for the fine tuning of light signal transduction at several checkpoints, including the degradation of active phyA mediated by the ubiquitin/26S proteasome pathway; the interaction of light-signaling positive factors with COP1, an E3 ubiquitin-protein ligase functioning as a nega-tive regulator of photomorphogenesis (Seoet al., 2004), re-ducing the affinity of phosphorylated phyA to its signaling partners (Kim et al., 2004) and controlling the phospho-rylation level and, consequently, the signaling activity, of phy (Ryuet al., 2005). Extensive functional conservation in angiosperms phosphorylation and post-translational pro-tein modification suggests that the transcripts identified in citrus are involved in the proteolytic degradation of light-signaling components.

Phot signal transduction components

Figure 5- Light-signaling associated bHLH transcriptional regulator family in citrus.A.schematic representation of phytochrome-regulated PIF3 transcriptional activation.B.alignment of the bHLH DNA-binding domainPIF/PIL family inArabidopsisand citrus. C. phylogenetic analysis of plant

Figure 6- Proteolysis-mediated photomorphogenesis control pathway in citrus.A.alignment of positive photomorphogenesis regulator families

HY5/HYH and LAF1.B.alignment of negative photormorphogenesis regulator families EID1 and SPA1. Dark and light gray shading indicate sequence identity and similarity, respectively. At,Arabidopsis thaliana; bZIP, basic leucine zipper; C, contig; CS,Citrus sinensis; CR,Citrus reticulata; PT,

Concluding Remarks

This preliminary survey of citrus photoperception-associated genes has provided useful information for fur-ther studies of light developmental control in these species. It has allowed the identification of conserved members of light-triggered signaling in a non-model species and the elaboration of a work model frame for light perception and signaling in citrus (Figure 7). These prospects are particu-larly attractive considering the range of economically im-portant physiological processes of citrus that are regulated by light, including secondary metabolism regulation and shading responses. An immediate goal of plant genomics is to transfer knowledge between model and crop species, al-lowing a better understanding of the mechanisms underly-ing several aspects of plant physiology. Thus, genomic and functional information can be integrated into the accumu-lated knowledge of citrus genetics and physiology to ad-vance basic and applied research. These studies will help to elucidate the molecular basis of developmental plasticity and to understand how environmental factors modulate plant development and the expression of phenotypic char-acters. The results obtained provide a new perspective on several aspects of light-regulated physiological processes

in citrus, such as de-etiolation, seedling establishment and shade-avoidance response.

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Supplementary Material

The following online material is available for this ar-ticle:

Table S1

Table S2 Table S3

Supplemental References Figure S1

This material is available as part of the online article from http://www.scielo.br/gmb.

Namea Gene ESTb %c e value biological process References

CRY1 AT4G08920 C10-CR (2)

CS00-C1-100-038-A12-CT

23.3 74.6

3e-91 1e-106

FAD binding domain, DNA photolyase, B photoreceptor, photomorphogenesis,

circadian clock entrainment, photoperiodic responses

Cashmore et al., 1999

CRY-DASH AT5G24850 C2-CR/CS (13)

C3-CS (4) C11-CS (3) C13-CA (2) PT11-C1-901-056-H09-CT 23.5 22.2 21.2 64.1 12.7 1e-93 1e-89 2e-87 1e-106 1e-62

Cryptochrome family, putative B photoreceptor, transcriptional regulator in

Synechocystis

Brudler et al., 2003, Kleine et al., 2003

PHOT1 AT3G45780 C8- CS (5)

CS00-C3-701-104-B03-CT CS00-C3-702-030-D01-CT CR05-C3-701-091-E08-CT CS00-C1-100-062-A04-UV PT11-C1-900-012-G11-CT 19.8 50.0 50.0 18.0 37.8 17.0 1e-56 4e-84 7e-54 6e-53 1e-53 2e-45

LOV1 and LOV2 domain, serine-threonine kinase domain, B photoreceptor, phototropism, chloroplast

movement, stomata opening control

Huala et al., 1997

PHOT2 C12-CS/PT (17)

C7-CS (7) C9-CS (2) C1-CR/CS (2) C4-CR/CS (2) CS00-C3-701-104-B03-CT CS00-C1-100-124-G03-CT 71.1 33.4 38.1 27.4 17.5 47.5 42.1 7e-94 5e-69 3e-63 4e-59 3e-38 4e-84 6e-74

phototropin family Jarillo et al., 2001

PHYA AT1G09570 CS00-C3-701-101-C11-CT

CS00-C3-705-056-G06-CT

58.3 34.7

6e-86 4e-81

PAS1, PAS2, chromophore binding domain, HKL domain, R/FR

photoreceptor

Sharrock and Quail, 1989

PHYB AT2G18790 CR05-C1-102-036-H07-CT

CS12-G8-000-003-D03-CT

15.3 8.1

3e-75 3e-55

phytochrome family Reed et al., 1993

FKF1 AT1G68050 C5-CS (2)

C6-CR/CS (3)

76.3 19.3

1e-142 1e-46

Kelch repeats, F-box domain, LOV domain, putative photoreceptor, photoperiodic flowering control,

circadian clock

Nelson et al., 2000

LKP2 AT2G18915 CS00-C3-702-030-D01-CT 22.0 1e-76 putative photoreceptor, circadian clock Schultz et al., 2001

ZTL AT5G57360 C5-CS 29.7 8e-71 putative photoreceptor, circadian clock Somers et al., 2000 a

Gene name abbreviations: CRY: cryptochrome; DASH: Drosophila, Arabidopsis, Synechocistis, human; PHOT: phototropin; PHY: phytochrome, FKF1: F-box, Kelch repeat, Flavin-binding protein1; LKP2: LOV domain, Kelch repeat protein2; ZTL: zeitlupe.

b

C: contig, CA: Citrus aurantium, CG: Citrus aurantifolia, CR: Citrus reticulata, CS: Citrus sinensis, LT: Citrus latifolia, PT: Poncirus trifoliata, (number of reads). c

Identity percentage at the amino acid level. d

Name Gene EST % e value biological process Reference ATHB2 AT4G16780 C6-CS/PT (23)

CS00-C2-003-056-F03-CT

40.1 27.5

3e-51 2e-34

homeobox leucine zipper, shade avoidance response

Carabelli et al., 1996

COP1 AT2G32950 C5-CS/CG (5) C2-CS (2) CA26-C1-002-001-E08-CT 81.9 65.1 40.4 1e-89 3e-78 9e-61

E3 ubiquitin ligase, Zn finger and RING finger domains, proteolysis

Osterlund et al., 2000, Seo et al., 2004

COP8/FUS4 /FUS8

AT5G42970 CS00-C3-702-101-D09-CT CR05-C1-102-033-G01-CT CA26-C1-002-037-H04-CT

2e-75 2e-72 7e-69

subunit 4 of COP9 signalosome complex, subunit of the 19S regulatory particle of the

26S proteasome

Serino et al., 1999

COP9/FUS7 AT4G14110 C1-CS (3) LT33-C1-003-023-F05-CT

21.9 28.0

3e-66 2e-56

COP9 signalosome subunit, identical to cDNA CSN complex subunit 8 (CSN8)

Dohmann et al., 2005

COP10/FUS9 AT3G13550 C2-CR/CS (6) C3-CS/PT (23) C4-CR/CS (8) CR05-C1-102-060-B12-CT 64.8 39.0 39.0 38.5 5e-69 5e-41 1e-40 1e-39

ubiquitin-conjugating enzyme (COP10), proteolysis

Yanagawa et al., 2004

COP11/FUS6 AT3G61140 C1-CS/PT(2) 16.9 2e-86 COP9 signalosome complex subunit 1 / CSN complex subunit 1 (CSN1) / COP11 protein

(COP11) / FUSCA protein (FUS6)

Kang et al., 2000

EID1 AT4G02440 C1-CS/PT (5) 22.0 7e-51 Cyclin-like F-box protein, protein degradation, photomorphogenesis

Marroco et al., 2006

FAR1 AT4G15090 C9-PT (2) CS00-C1-100-058-F05-CT

37.3 32.7

1e-29 5e-35

FAR1 family, transposase-like domain Hudson et al., 1999

FHY3 AT3G22170 C9-PT (2) CS00-C1-100-058-F05-CT

34.2 24.6

1e-29 1e-33

FAR1 family, transpose-like domain Wang and Deng, 2002, Lin and Wang, 2004

FHY1 AT2G37680 CR05-C1-100-082-A02-CT CS00-C1-100-124-B05-CT CR05-C3-700-106-G10-CT CS00-C1-102-029-H04-CT 68.3 58.7 58.3 18.3 2e-71 2e-71 2e-71 2e-70

no recognizable domain, phyA-mediated photomorphogenesis

Shen et al., 2005a

HAF2 AT3G19040 C3-CA/CR (2) 47.5 2e-56 TATA-binding protein-associated factor TAF1 (TAFII250), bromodomain, ubiquitin

domain, histone acetyltransferase activity

Bertrand et al., 2005

HFR1 AT1G02340 C6-CG/LT (2) 29.4 4e-32 transcriptional regulator, bHLH domain, de-etiolation

Duek and Fankhauser, 2003

HY5 AT5G11260 CS00-C1-650-014-E02-CT 17.9 1e-35 transcription regulator, bZIP DNA binding domain, photomorphogenesis

Chattopadhyay et al., 1998

HYH AT3G17609 CS12-G8-000-020-G07-CT 16.1 2e-42 transcriptional regulator, bZIP DNA binding motif

Holm et al., 2002

LAF1 AT4G25560 C6-CS/PT (2) C3-CS (2) C5-CR (2) 73.9 67.4 63.0 2e-78 1e-68 6e-62

MYB transcription factor, R2R3 group, de-etiolation

C2-CS (2 45.3 1e-46 protein, histidine kinase, phy- and auxin-mediated signal transduction

Choi et al, 2005

PAP1 AT1G56650 C3-CS (2) CR05-C3-700-042-H12-CT CR05-C3-700-004-E04-EU PT11-C1-900-084-F06-CT 28.6 28.2 25.4 24.6 5e-56 2e-58 1e-55 1e-49

transcriptional regulator, auxin responsive, anthocyanin biosynthesis

Teng et al., 2005

PFT1 AT1G25540 C1-CG/CS (2) C2-CS/CR (6)

28.4 65.4

1e-97 1e-148

von Willebrand factor type A (VWF-A), glutamine-rich C-terminal, flowering time

Cerdán and Chory, 2003

PIF3 AT1G09530 C6-CG/LT (2) 25.5 4e-27 transcriptional regulator, bHLH domain, photomorphogenesis

Ni et al., 1998, Ni et al., 1999

PIF4 AT2G43010 C6-CG/LT (2) 24.5 1e-22 PIF family, transcriptional regulator, bHLH domain, de-etiolation (cell expansion)

Huq and Quail, 2002

PKS1 AT2G02950 C1-CR/CS (2) 20.2 1e-18 no recognizable domain, phytochrome kinase substrate,

Lariguet et al., 2003

PP7 AT5G63870 C3-CS/CR/PT (3)

C12-CS (11) CS13-C1-001-008-C12-CT PT11-C9-005-041-C05-CT 29.6 23.5 25.3 23.9 2e-55 7e-45 9e-46 1e-42 metallo-phosphoesterase motif, serine/threonine specific protein phosphatases

signature, de-etiolation

Møller et al., 2003

RAP1 / ATMYC2 AT1G32640 C2-CR/CS (2) CR05-C3-701-055-H07-CT

25.8 39.5

1e-39 4e-42

MYC-related transcriptional activator, bHLH leucine zipper motif, photomorphogenesis.

Heim et al., 2003

RFI2 AT2G47700 C1-CS (3) 34.5 4e-39 zinc finger (C3HC4-type RING finger) family protein, photomorphogenesis

Chen and Ni, 2006

SPA1 AT2G46340 C7-CR (3) C5-CR/CS/PT (3) CS13-C1-001-017-G02-CT 32.2 25.6 26.8 1e-114 2e-31 4e-31

proteolysis targeting, WD-repeat domain, light-regulated proteolysis

Höcker et al., 1999, Laubinger et al., 2004

SHB1 AT4G25350 C1-LT/CS (3) PT11-C1-900-042-H02-CT

27.8 17.1

2e-53 2e-25

EXS domain, SPX domain, photomorphogenesis under B

Kang and Ni, 2006

SUB1 AT4G08810 C3-CG/CS/PT (11) PT11-C1-901-057-B05-CT

37.0 22.4

2e-64 5e-44

Ca+2-binding protein, de-etiolation Guo et al., 2001

a_{Gene name abbreviations: ATHB: Arabidopsis thaliana homeobox; ATMYC: Arabidopsis thaliana MYC-type; COP: constitutively photomorphogenic ; EID: Eimpfindlicher Im Dunkelroten}

Licht; FAR: far-red impaired response; FHY : far-red elongated hypocotyl ; FUS: Fusca; HAF: histone acetylation factor; HFR : long hypocotyl in FR light ; HY: long hypocotyl; HYH :

HY5-homologue; LAF: long after far red; NDPK: nucleotide diphosphate protein kinase; PAP: production of anthocyanin pigment; PAT: phytochrome A-signal transduction ; PFT:

phytochrome and flowering time; PIF: phytochrome-interacting factor; PP: protein phosphatase ; RAP:ethylene response factor subfamily B-4 of ERF/AP2 transcription factor family; RFI:red and far red insensitive ; SPA: suppressor of phytochrome A-105; SHB: short hypocotyl under blue; SUB: short under blue.

b_{C: contig, CA: Citrus aurantium, CG: Citrus aurantifolia, CR: Citrus reticulata, CS: Citrus sinensis, LT: Citrus latifolia, PT: Poncirus trifoliata, (number of reads).} c_{Identity percentage at the amino acid level;}

d_{Functional domains abbreviations: ATP: adenosine triphosphate; bHLH: basic helix-loop-helix; bZIP: basic Zipper; FAD: flavina adenosine dinucleotide; HKL: histidine kinase-like; LOV:}

Name

Gene

EST

%

e value

biological process

Reference

ARF7/

NPH4

AT5G20730

C4-CR

C1-CS/CR

CS00-C3-705-071-D01-CT

55.1

41.5

47.8

1e-89

3e-62

5e-93

B3 DNA binding domain,

AUX/IAA family, auxin-regulated

transcription

Harper

et al.

,

2000

GRF1

and

GRF

family

AT4G09000

C2-CS

C4-CS

C9-CA/PT

C10-CA/CS

CS00-C1-101-018-E05-CT

CS00-C3-700-041-F04-CT

71.1

64.3

51.6

52.2

39.5

29.9

1e-113

1e-104

4e-99

1e-102

1e-101

2e-97

regulatory factor1-G-box factor

14-3-3 homolog isoform family,

signal transduction (scaffolding)

Ferl, 2004

NPH3

and

NRL

family

AT5G64330

C5-CS

C6-CR

C8-CR/CS

CS00-C3-701-013-G03-CT

CS00-C3-701-060-E12-CT

PT11-C1-900-042-G09-CT

PT11-C1-900-043-E10-CT

47.1

21.6

19.3

25.2

35.4

39.3

33.3

9e-71

3e-59

4e-59

6e-82

5e-96

1e-78

4e-67

plant-specific NPH3 domain,

BTB/POZ domain, signal

transduction (scaffolding)

Motchoulski and

Liscum, 1999,

Haga

et al.

, 2005

PIN1

and

PIN

family

AT1G73590

C3-CG/CS

C11-CA/CS

CS00-C3-700-106-C03-CT

23.4

24.6

38.7

2e-75

3e-89

4e-97

auxin efflux carrier, tropic

responses

Blakeslee

et al.

,

2004

RPT2

AT2G30520

C1-CS

C7-CR

CS00-C3-702-027-G06-CT

27.6

70.8

18.3

2e-65

1e-132

4e-42

plant-specific NPH3 domain,

BTB/POZ domain, signal

transduction (scaffolding)

Inada

et al.

, 2004

a

Gene name abbreviations: ARF: auxin-responsive factor ; GRF:general regulatory factor (14-3-3 protein) ; NPH: non-phototropic hypocotyl ; PIN: pin-formed ; RPT: root phototropism.

b

C: contig, CA: Citrus aurantium, CG: Citrus aurantifolia, CR: Citrus reticulata, CS: Citrus sinensis, LT: Citrus latifolia, PT: Poncirus trifoliata, (number of reads).

c

Identity percentage at the amino acid level.

d

photoperception and light signal transduction according to gene ontology (GO)

categories in comparison to

Populus trichocarpa

transcriptome and

Arabidopsis

thaliana

proteome.

A.

cellular component.

B.

molecular function. Assignments are

based on the data available at the TIGR

Arabidopsis thaliana

Gene Index version